rethinking sediment biogeochemistry after the discovery of electric currents

MA07CH21-Nielsen ARI 11 September 2014 14:18

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Rethinking SedimentBiogeochemistry After theDiscovery of Electric CurrentsLars Peter Nielsen and Nils Risgaard-PetersenSection for Microbiology and Center for Geomicrobiology, Department of Bioscience,Aarhus University, 8000 Aarhus C, Denmark; email: [email protected],[email protected]

Annu. Rev. Mar. Sci. 2015. 7:21.1–21.18

The Annual Review of Marine Science is online atmarine.annualreviews.org

This article’s doi:10.1146/annurev-marine-010814-015708

Copyright c© 2015 by Annual Reviews.All rights reserved

Keywords

cable bacteria, electric fields, sulfide, carbonates, iron

Abstract

The discovery of electric currents in marine sediments arose from a simpleobservation that conventional biogeochemistry could not explain: Sulfideoxidation in one place is closely coupled to oxygen reduction in anotherplace, centimeters away. After experiments demonstrated that this resultedfrom electric coupling, the conductors were found to be long, multicellular,filamentous bacteria, now known as cable bacteria. The spatial separationof oxidation and reduction processes by these bacteria represents a shortcutin the conventional cascade of redox processes and may drive most of theoxygen consumption. In addition, it implies a separation of strong protongenerators and consumers and the formation of measurable electric fields,which have several effects on mineral development and ion migration. Thisarticle reviews the work on electric currents and cable bacteria publishedthrough April 2014, with an emphasis on general trends, thought-provokingconsequences, and new questions to address.

21.1

Review in Advance first posted online on September 19, 2014. (Changes may still occur before final publication online and in print.)

Changes may still occur before final publication online and in print

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THE DISCOVERY OF ELECTRIC CURRENTS IN MARINE SEDIMENTS

A Conventional Observation with No Conventional Explanation

Electric currents in marine sediments were discovered by chance, as a spin-off from a series ofexperiments on nitrate-storing, filamentous sulfur bacteria (Sayama et al. 2005). In one experiment,glasses with homogeneous, sulfidic sediment were incubated with overlying oxic water, and after30 days, a centimeter-wide zone with no detectable oxygen or pore-water sulfide had developed(L.P. Nielsen & N. Risgaard-Petersen, unpublished data) (Figure 1). Many mechanisms cangenerate and maintain these so-called suboxic zones, and in coastal marine sediments, they appearto be the rule rather than the exception (Canfield et al. 1993, Fenchel et al. 2012, Preisler et al.2007). In this specific experiment, however, all known explanations were ruled out. Oxidation orprecipitation of sulfide with iron was rejected because the sediment was saturated with sulfide tobegin with, no animals were present that could mix down new ferric iron from the oxic zone, andcontrol cores with no oxygen showed no depletion of sulfide. No intrusions of oxic water couldoccur in this fine-grained sediment without animals, and no nitrate that could have oxidized sulfidebelow the oxic zone was present. The experiment was highly reproducible, and experimentalerrors and instrument problems were carefully excluded. Something beyond the then-presentunderstanding of sediment biogeochemistry was evidently going on.

Eventually, the idea of electron transport through the sediment emerged. The observed sep-aration of oxygen and sulfide was readily explained if the sediment contained conductors that

O2 + 4 H+

2 H2O e–

4 H2O +H2S

SO42– + 10 H+

e–

0 100 200 300

O2 (μM)

–5

0

5

10

15

20

25

300 10 20 30 40 50

6.0 7.0 8.0 9.0

pH

∑H2S (μM)

∑H2S

Dep

th (m

m)

O2

pH

Figure 1Combined profiles of oxygen, sulfide, and pH along with the electrochemical reactions. Adapted fromNielsen et al. (2010) and Risgaard-Petersen et al. (2012).

21.2 Nielsen · Risgaard-Petersen


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could direct electrons from sulfide oxidation at depth to oxygen reduction at the surface. Strongindependent confirmation came from pH profiles that showed distinct proton consumption in theoxic zone, which was consistent with electrochemical, cathodic oxygen reduction and not with anyother known processes in a dark, oxic sediment zone (Nielsen et al. 2010) (Figure 1). A third lineof evidence came from manipulations showing that the pore-water sulfide distribution respondedto changes in oxygen concentration much more quickly than could be explained by the diffusionof any compound from the oxic to the sulfidic zone (Nielsen et al. 2010).

Finding the Cables

The discovery of electric currents in marine sediments was followed by an intensive search for theelectron conductor in the sediments. The first hypothesis was a network of bacterial nanowiresin combination with semiconductive mineral grains or humic particles, as was proposed at thesame time for biogeobatteries (Nielsen et al. 2010, Revil et al. 2010) (see sidebar, Geobatteriesand Biogeobatteries, along with Figure 2). The immediate halt of the electric current at a cutalong the oxic-anoxic interface confirmed that the conductor was a solid structure. Additionalexperiments with filter barriers at the oxic-anoxic interface indicated that the conductive structurewas engineered by ordinary-size bacteria, as no electric currents developed if the pore size of the

H2OO2

NO3–

N2

Electrons

Electrons

Pili

Pili

Bacteria

Bacteria

CathodeElectron sink area

MineralsElectronic conductor

or semiconductor(e.g., FeS, hematite)

OrganicsCO2

AnodeElectron source area

Figure 2Proposed mechanisms of electron transfer from reduced to oxic zones in a contaminated aquifer. Differentbacterial cells capable of extracellular electron transfer are connected in a network of microbial nanowiresand/or grains of semiconductive minerals to make a biogeobattery. The electron transport may also involveexternal electron shuttles. Adapted from Revil et al. (2010).

www.annualreviews.org • Electrifying Sediments 21.3


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GEOBATTERIES AND BIOGEOBATTERIES

Geobatteries are large, natural electric-current generators in which a conductive pyrite ore body crossing twodifferent redox domains transports electrons from the anodic oxidation reactions at depth to the cathodic reductionreactions near the surface. The surrounding soil acts as an electrolytic conductor, with charge transport by ionmigration completing the electric circuit and maintaining charge balance (Sato & Mooney 1960). This model hasbeen recognized as an explanation for the natural electric fields (referred to as self-potential anomalies) observedin the vicinity of conductive ore bodies. Redox-associated electric fields have also been observed at field sitescontaminated by landfill leachate and chlorinated organic solvents (Arora et al. 2007; Naudet et al. 2003, 2004).The suggested mechanism is a biogeobattery in which bacteria, either alone or in connection with mineral particles,act as electron conductors and the redox processes are catalyzed biologically (Revil 2010) (Figure 2).

filter was below 0.8 μm (Pfeffer et al. 2012). Yet it was a surprise when the conductor appearedto be not a collective network connecting many different bacteria but simply long, thin, filamen-tous bacteria controlling both the cathodic and anodic reactions and the associated long-distanceelectron transport (Pfeffer et al. 2012) (Figure 3).

All cells in these multicellular bacteria share the outer membrane, and within the commonperiplasmic space many parallel strings are embedded. Continuity along the entire filament andexceptional charge mobility suggest that these strings are the electric wires (Pfeffer et al. 2012).In appearance and function, these filaments bear a striking resemblance to electric cables, andthey have therefore been named cable bacteria (Pfeffer et al. 2012, Schauer et al. 2014). Allcable bacteria identified so far are closely related (>95% 16S DNA sequence identity), and theirnearest cultivated relative is Desulfobulbus propionicus, within the Desulfobulbaceae family (92%identity). How the strings function as electron conductors at the molecular level has not beendetermined. Efforts to connect the cable bacteria with electrodes and an external circuit havefailed so far, and the limits of their current strength, voltage span, and conductivity have not beensettled.

Implications of Microbial Electric Currents

The separation of cathodic and anodic processes by cable bacteria has several important impli-cations for biogeochemistry, which we discuss below. In short, this separation challenges theconventional thinking that (a) both electron donors and acceptors for a metabolic process need tobe in the same cell, or at least within a few micrometers of each other [i.e., the reach of extracellularelectron exchange by microbial nanowires or electron shuttles (Reguera 2012)]; (b) pH excursionsare restrained by the net proton balance of complete redox and dissolution-precipitation processes;and (c) electric fields do not develop in marine sediments, or at least not to a magnitude influencingthe ion fluxes and kinetics of biogeochemical processes.

ELECTRON DONORS AND ACCEPTORS

Sulfide Sources

Electrons in the electric currents in marine sediments are donated by three different sulfide sources:pore-water sulfide diffusing up from sulfate reduction in underlying zones, sulfide produced locallyby sulfate reduction, and sulfide produced by iron sulfide dissolution. Their relative importancevaries with the type of environment and succession stage. Pore-water sulfide is initially the only



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1.17 μm 1.10 μm

a b

c

400 nm10 μm

5 μm5 μm

Figure 3Cable bacteria. (a) Filamentous Desulfobulbaceae identified by fluorescence in situ hybridization targeting 16S rRNA. Filament cellsappear yellow because of the overlay of images obtained with probe DSB706 (labeled green) and probe ELF654 (labeled red ).(b) Thin-section transmission electron microscopy images of filament cross sections. (c) Scanning electron microscopy image of twoadjacent filaments.

source, donating electrons when sulfidic sediments are exposed to oxygen and cable bacteria beginto establish (Schauer et al. 2014). The two other sources come into play after a separation of theoxic and sulfidic zones appears. Direct measurements of Aarhus Harbor sediment after 45 days ofincubation showed iron sulfide to be the main source (94%), followed by local sulfate reduction(5%) and diffusion (<1%) (Risgaard-Petersen et al. 2012) (Table 1). A time-series study withsimilar sediment likewise found that the contribution of diffusion declined to 30% after 10 daysand to 6% after 53 days (Schauer et al. 2014) (Table 1). In another time-series study lasting 47 days,no pore-water sulfide was detectable at any time in the top 30 mm of the sediment (Malkin et al.2014). In contrast to these results, Larsen et al. (2014) found that diffusion was responsible for



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Table 1 Biogeochemical characteristics of sediments with electric currents

Current minimum Sulfide sourcea

Location SeasonIncubation

(days)

O2-H2Ssepara-

tion(mm)

SOD(mmolO2 m−2

d−1)(mAm−2)

(% ofSOD)

Diffusion(%)

LocalSRR (%) FeS (%) Reference

Laboratory

Harbor NA 30 19 46 86 42 6 94 Nielsen et al.2010Bay 30 12–19 10 14 31 87 13

Harbor 45 12 35 66 47 <1 5 94 Risgaard-Petersen

et al. 2012

Bay 21–28 12 NR Pfeffer et al.2012

Bay 10 7 21 68 81 30 70 Schauer et al.201413 16 38 92 61 NR

21 19 23 56 61

53 22 12 12 25 6 94

Harbor 10 17 NR NR Risgaard-Petersen

et al. 20148 18

14 25 104 381b 82

Harbor 19 18 67 180 67 NR Damgaardet al. 2014

In situ

Intertidal June NA NR 30 30 23 NR Malkin et al.2014February 20 7 8

NR 12 NR

Subtidal October NR 32 25 19

March 25 5 5

NR 16 NR

Marine lake November NR 44 25 14

January 14 16 30

February 22 27 34

NR 10 NR

Abbreviations: NA, not applicable; NR, not reported; SOD, sediment oxygen demand; SRR, sulfate reduction rate.aValues spanning two columns represent the sum of both (local SRR + FeS).bEstimated from electric potential gradient.

92% of the contribution in sandy salt marsh sediments even after 35 days of incubation, possiblyowing to the small amount of iron sulfide in comparison with the organic content.

This variability suggests a distinction between (a) ephemeral blooms of cable bacteria associatedwith iron sulfide pools that become accessible and rapidly depleted and (b) more persistent andactive cable bacteria communities that are fueled by continuous sulfate reduction arising fromburied organic matter. As discussed below, the pool of calcite buffering the anode process mayeventually determine the temporal limits when cable bacteria may operate.



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Other Electron Donors and Acceptors

Marzocchi et al. (2014) recently established that electric currents and cable bacteria may develop insediments where oxygen in the overlying water has been replaced with nitrate. Several pathways ofdissimilative nitrate reduction are known, with nitrite as a universal first product and subsequentreduction to ammonium and dinitrogen as separate routes, with nitric oxide and nitrous oxideas free intermediates in the latter. Other experiments have shown that nitrite also stimulates theelectric currents, thus leaving open the possibility that nitrite reduction (and not necessarily thefirst nitrate reduction) is the direct cathodic process (Risgaard-Petersen et al. 2014). Dinitrogenis unlikely to be the end product because parallel incubations with an intermediate (nitrous oxide)had no effect. DNA sequence data have suggested that oxygen- and nitrate/nitrite-reducing cablebacteria are identical (Marzocchi et al. 2014), and this was confirmed by the experiments demon-strating that replacing the oxygen in the overlying water with nitrate did not stop the electriccurrents.

An intriguing and open question, then, is what a cable bacterium does when both oxygen andnitrate are present in the overlying water. Does it have controls ensuring that electrons fromthe anodic process at depth are not captured by cells in the nitrate reduction zone, and insteadare passed on to the cells in the oxic zone and used primarily in the energetically more favorableoxygen reduction? This question is one more reminder of how much is left to learn about thecontrols and kinetics of the electrochemical reactions and their interactions with live wires.

Reactive ferric iron reacts abiotically and rapidly with sulfide, and therefore it seems that theprocess is not used biologically in sediments (Fenchel et al. 2012) Cable bacteria could overcomethis obstacle by keeping the reactants apart and using electrical connections to compete withthe spontaneous reaction. So far, however, no observations or tests have indicated that cablebacteria can in fact switch to ferric iron when more potent electron acceptors are removed. Studieshave repeatedly shown that, even with plenty of reactive ferric iron in the oxic zone (Risgaard-Petersen et al. 2012), removing oxygen halts electric currents immediately, with no recoverywithin observation periods of up to 24–33 h (Pfeffer et al. 2012, Risgaard-Petersen et al. 2012).Iron reduction depends on extracellular electron transfer because of the low solubility of ferriciron compounds, and the negative results of iron reduction tests do not exclude the possibility thatsome cable bacteria can use extracellular electron exchange in another context.

Before the importance of iron sulfide as an electron donor was discovered, Nielsen et al. (2010)proposed that organic carbon could be the important electron donor in the suboxic zone. The factthat the closest relative to identified cable bacteria is a sulfate-reducing organotroph, Desulfobulbuspropionicus (Pfeffer et al. 2012), also suggests that organic carbon plays a direct role as an electrondonor for cable bacteria. However, no experimental results or observations have confirmed thispossibility so far, and studies in organic-rich sediments have obtained complete electron massbalances only with sulfide as the electron donor (Risgaard-Petersen et al. 2012).

GEOCHEMICAL AND GLOBAL IMPLICATIONS

The presence of bioelectric currents may significantly complicate the classical view of how keyelements like iron, carbon, calcium, and sulfur are cycled. According to this view, oxidative dis-solution of solid-phase iron sulfides depends on direct reactions with oxygen, nitrate, or oxidizedmetals (Aller & Rude 1988, Canfield et al. 1993, Schippers & Jørgensen 2002), which implies thatdissolution of subsurface iron sulfide necessitates physical mixing (for example, via bioturbation).Metabolically mediated carbonate dissolution occurs exclusively in oxic sediment layers throughCO2 formation from aerobic respiration and through proton formation from aerobic reoxidation



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Oxic zone

Sulfidic zone

FeS + 2 H+ Fe2+ + H2S

Org C + SO42– H2S

H2S + 4 H2O SO42– +10 H+ + 8 e–

CaCO3 + 2 H+ H2CO3 + Ca2+

Xred + O2 Xox + H+

Org C+ SO42– H2S

H2S + Fe2+ FeS/FeS2

Suboxic zone

4 H+ + 4 e– + O2

4 Fe(OH)3 + 8 H+4 Fe2+ + 10 H2O + O2

H2CO3 + CaxMg(1 – x)CO3xCa2+ + 2 HCO3– + (1 – x)Mg2+

Fe2+Fe2+

Fe2+Fe2+

Ca2+Ca2+

Ca2+Ca2+

e–

e–

2 H2O

e–

1.5 cm

a bb

Biogeochemical reactions

Transport

Figure 4(a) Oxidation, reduction, and dissolution processes in sediment bioelectric currents. Solid arrows represent biogeochemical reactions;dashed arrows represent transport (diffusion and drift). Cable bacteria transport the electrons from anodic sulfide oxidation to cathodicoxygen reduction and catalyze the reactions. Adapted from Risgaard-Petersen et al. (2012). (b) Sediment core with an approximately1.5-cm-deep, light gray zone where the black iron sulfide has been depleted. Above this zone, orange iron hydroxide has accumulated;below it, a darker gray band suggests the reprecipitation of iron sulfide. The core was incubated with an oxygenated water column inthe laboratory for two months.

of reduced metabolites transported into the oxic zone (Aller 1982, Walter et al. 1993); the for-mation of authigenic calcium and magnesium carbonates (such as magnesium calcite or dolomite)occurs in anoxic sediment layers like the sulfate-methane transition zone (Kelts & McKenzie 1982;Meister et al. 2007, 2011).

In sediments with significant bioelectric activity, iron sulfides and carbonates are dissolvedin the anoxic zone and their constituents (such as S2−, Fe2+, and Ca2++) are mobilized or con-sumed, whereas iron oxides and carbonates such as magnesium calcite are formed in the oxic zone(Risgaard-Petersen et al. 2012). These processes are tightly coupled to pH excursions from theanodic and cathodic reactions (Figure 4). Anodic sulfide oxidation induces sulfide depletion andproton formation in the suboxic zone, which promotes the dissolution of iron sulfides and mo-bilizes ferrous iron and sulfide. Anodic oxidation of the mobilized sulfide further accelerates thedissolution of iron sulfide, resulting in a positive-feedback mechanism whereby sulfide oxidationleads to a continuous supply of sulfide. The stoichiometry of this coupled dissolution-oxidationprocess even suggests a net production and accumulation of sulfide. Such accumulation has neverbeen observed in bioelectric sediments, however (Malkin et al. 2014, Nielsen et al. 2010, Schaueret al. 2014), probably because buried or authigenic carbonates act as proton sinks, acceleratingthe dissolution of these minerals (Risgaard-Petersen et al. 2012). In systems richer in iron sulfidethan in carbonate, the paradoxical accumulation of sulfide driven by sulfide oxidation may even-tually occur. It is also possible, however, that the carbonate pool may act as an important buffer,



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preventing the pH from dropping to critical physiological values; once this pool is depleted, thecable bacteria may die off.

The cathodic oxidation process consumes protons, which leads to an elevated pH in the oxiczone and a resulting carbonate precipitation. Iron mobilized from the iron sulfide pool also pre-cipitates as iron oxides in that zone. Eventually, in many laboratory-incubated sediments, a thickcrust of magnesium calcite and ferric iron forms at the sediment surface after a few weeks ofincubation (making microsensor work complicated and expensive).

The dissolution of carbonates associated with the anode process is probably much more impor-tant for the carbon fluxes than any direct or indirect interaction with organic carbon mineraliza-tion. The oxidation of one organic carbon molecule delivers roughly four electrons, and if they arepassed to the anode process via sulfate reduction and sulfide, approximately four protons are gen-erated. This in turn results in the dissolution of four carbonate carbon molecules. The carbonatedissolution is only partly balanced by carbonate precipitation in the oxic zone, as the consistentlyobserved pH peaks imply that the sediment as a whole is taking up protons or, rather, exportingalkalinity, thus indicating that net carbonate dissolution exceeds organic carbon oxidation. Eventemporary activities of cable bacteria may thus result in significantly less carbonate being buriedin the sediment: Total sulfate reduction in shallow-water marine sediments (<1,000 m) has beenestimated at approximately 70 × 1012 mol S y−1 ( Jørgensen & Kasten 2006), and if only 2% of theproduced sulfide is reoxidized by anodic oxidation buffered by carbonate dissolution, the carbonatedissolution rate becomes 11.2 × 1012 mol C y−1, assuming 8 electrons and protons generated persulfide-S oxidized. This rate is comparable to the estimated rates of total shallow-water carbonateburial and carbonate dissolution, 14.5 × 1012 and 10 × 1012 mol C y−1, respectively (Schneideret al. 2006). The electric currents might therefore be a hitherto overlooked mechanism sustainingocean alkalinity and the absorption of atmospheric CO2. The cycling of many other elementsand contaminants is coupled to the dissolution/precipitation of carbonates and sulfides, and ourunderstanding of these processes may also need revision in light of sediment electric currents.

ELECTRIC FIELDS

Cable bacteria generate an electric field in bulk sediment (Damgaard et al. 2014; Risgaard-Petersenet al. 2012, 2014) similar to that generated in geobatteries or biogeobatteries (see sidebar, Geo-batteries and Biogeobatteries, along with Figure 2). This field is generated because the verticallydispersed anodic and cathodic reactions of the bacteria promote a minor local charge imbalancein the environment, with the anodic site being more positively charged than the cathodic site(Figure 5). Although ionic transport in the pore water completes the overall electric circuit andhence tends to diminish the resulting field, the resistivity of the sediment implies that the fieldis not completely counterbalanced. The electric fields are manifested as a downward increase inelectric potential and are on the order of a few millivolts per centimeter (Damgaard et al. 2014;Risgaard-Petersen et al. 2012, 2014).

Electric potential microelectrodes have recently been developed to measure such small fieldsin marine sediments. An electric potential microelectrode is essentially an Ag-AgCl electrodemodified by (a) tapering of the tip to allow nondisturbing profiling in the sediment, (b) electricalshielding to allow measurements on a microvolt/millivolt scale, and (c) protection of the Ag-AgClhalf cell against intruding redox-active species from the environment (Damgaard et al. 2014). Thevariations in electric potential along a depth transect in the sediment are typically measured againsta reference electrode positioned in a fixed position, for example, in the water column overlying thesediments. The reference electrode can be either an identical electrode or a standard commercialAg-AgCl reference electrode. Figure 6 shows the distribution of electric potentials in marine



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SO42– + 10 H+

4 H2O + H2S

e–

SO42– + 10 H+

4 H2O + H2S

e–

SO42– + 10 H+

4 H2O + H2S

e–

2 H2O

O2 + 4 H+

Je Ji

e–

e–

e–

e–

e–

Cathode

Anode

Figure 5Conceptual illustration of cable bacteria in the sediment, with an emphasis on the electric circuit (electronand ion pathways). The cable bacteria catalyze both the half reaction of sulfide oxidation and the halfreaction of oxygen reduction and also act as electron conductors, transporting electrons between thereactions through isolated internal conductive structures. The return current pathway is via ionic chargecarriers in the surrounding pore-water fluid. Adapted from Risgaard-Petersen et al. (2014).

sediments as measured with an electric potential microelectrode, along with microprofiles ofoxygen, sulfide, and pH.

The presence of an electric field generated from cable bacterial activity in the sediment hasimplications for the transport of ions. The field exerts a force on the ions such that cations migratein the direction of the field and anions migrate in the opposite direction (Bockris & Reddy 1998).This ion migration represents a supplement to other transport mechanisms, such as moleculardiffusion and advection, and should be included when estimating ion fluxes from concentrationprofiles in electric coupled systems. Risgaard-Petersen et al. (2012) recently showed that ignoringthe field-driven ion migration in such a system led to an almost 50% overestimation of the flux ofSO2−

4 toward the sediment surface and to a 15% underestimation of the Ca2+ flux. The inclusion



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–5

0

5

10

15

20

pH

Dep

th (m

m)

O2 pH

O2, Stot (μM)2–

Electric potentialS tot2–

0 50 100 150 200 250 300

6.0 6.5 7.0 7.5 8.0 8.5 9.0

Electric potential (mV)

0.0 0.5 1.0 1.5 2.0

Figure 6Electric potential gradient associated with biogeoelectric currents in a sediment core, as measured with anelectric potential microelectrode. Oxygen, sulfide, pH, and electric potential microprofiles were measuredafter 19 days of incubation in the presence of an aerated overlying water column. The sediment displayedsignatures typical of the presence of cable bacteria (i.e., a pH peak in the oxic zone and an approximately20-mm-wide suboxic zone with no detectable sulfide). The electric potential increased from zero at thesediment surface to +1.85 ± 0.1 mV at depths of 18.5 mm and greater. The zone where the electricpotential changes corresponds well with the zone depleted in pore-water sulfide. Adapted from Damgaardet al. (2014).

of ion migration can be obtained by using the Nernst-Planck equation (Bockris & Reddy 1998),modified for estimating ion fluxes in sediment (Risgaard-Petersen et al. 2012):

J = −φDs ·(

dCdz

+ (±1)nFRT

Cdψ

dz

), (1)

where J is the flux in the vertical direction, φ is the sediment porosity, Ds is the self-diffusioncoefficient of the ions in the sediment, dC/dz is the concentration gradient, dΨ /dz is the electricpotential gradient (−dΨ /dz corresponds to the electric field), n is the number of charges, F is theFaraday constant, R is the gas constant, and T is the absolute temperature.

Another feature of the presence of a field generated from cable bacteria activity is a skewness inthe microdistribution of conservative ions, such as Na+ and Cl−. In a quasi-steady-state situation,



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these ions tend to distribute with opposing concentration gradients according to Equation1. This unusual distribution might be taken as an indication of the presence of bioelectriccurrents.

The electric field can be used to estimate the electric current generated by the cable bacteria(Risgaard-Petersen et al. 2014). We can consider the cable bacteria–sediment system to be a closedelectric circuit with electron and electrolytic conductors: The cable bacteria represent the electronconductors, and the surrounding bulk sediment represents the electrolytic conductors (Figure 5).In such a system, the ionic current in the electrolytic conductor is equal in magnitude but oppositein direction to the current in the electron conductor(s) (Bockris & Reddy 1998). The electroncurrent that is produced by and runs in the cable bacteria can therefore be quantified from thecorresponding ionic current. The density of the ionic current can be estimated from the magnitudeof the electric field and the resistance of the sediment by means of Ohm’s law (Revil et al. 2010,Risgaard-Petersen et al. 2014):

Ji = −σ ·(

dψ

dz

), (2)

where Ji is the density of the ionic current (in units of amperes per square meter), σ is the ionicconductivity of the bulk sediment [in units of siemens (S) per meter], and dΨ /dz is the electricpotential gradient (in units of volts per meter; note that −dΨ /dz corresponds to the electric field).From the data presented in Figure 6, this approach yields an electron current density near theoxic-anoxic interface of 298 mA m−2 when a conductivity of 1.75 S m−1 is assumed (estimated fromArchie’s law according to Ullman & Aller 1982; see Damgaard et al. 2014). This current densityis almost twice as high as the minimum current density estimated from the proton-oxygen massbalance model of Nielsen et al. (2010) (i.e., 180 mA m−2), probably because the proton-oxygenmass balance does not take into account the pH buffering by carbonate precipitation (Risgaard-Petersen et al. 2012) and also because of the pH microsensor’s limitations in resolving the realsteepness of the pH gradients at the borders of the narrow oxic zone.

The above approach assumes that the charge transfer via the cathodic and anodic reactionsperformed by the cable bacteria is the only significant source of the electric field (which was thecase for the example above). In nature, however, electric fields from other sources may exist.Among others, these may include the field generated from the diffusion of cations and anions withdifferent diffusion coefficients (diffusion potentials) and, in the case of pore-water flow, anotherfield of electrokinetic nature—a streaming potential field (for a review, see Revil et al. 2012).The diffusion potential exemplifies the magnitude and potential impact of such sources: Chloridediffuses approximately 1.56 times faster than Na+, implying an electric potential difference of12 mV for every 10-fold difference in NaCl concentration between two sites (Bockris & Reddy1998). A change in salinity by only 10% in the overlying water thus induces a difference in electricpotential of 0.55 mV, which is comparable to the electric field generated by microbial electriccurrents (Figure 6).

Experimental procedures are available that can identify the electric field generated by cablebacterial activity and isolate it from those generated by other sources. One such procedureis to compare electric fields measured before and immediately after experimental inhibitionof cable bacterial activity. This inhibition can be created either by the instant removal of keyelectron acceptors like oxygen (Risgaard-Petersen et al. 2014)) or by a horizontal cut of the cablebacteria near the oxic-anoxic interface (Pfeffer et al. 2012). Combined with such procedures,electric potential measurements represent a strong, simple tool for assessing the presence andmagnitude of bioelectric currents generated by cable bacteria, making it possible to performdetailed ecophysiological and biogeographic studies of a unique microbial community.



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In general, electric fields in sediments should be more pronounced and important at lowersalinities because the ionic conductivity is lower and the diffusion potentials are controlled byrelative and not absolute differences in ion concentrations. Electric potential differences in therange of several hundred millivolts have indeed been measured above contaminated terrestrialaquifers and have been proposed to indicate electric microbial activity (Revil et al. 2010). FollowingBaas Becking’s (1934) hypothesis that “everything is everywhere, but the environment selects,”we would not be surprised if cable bacteria have a much broader cosmopolitan distribution thanhas been anticipated so far, including in limnetic and terrestrial environments.

ABILITIES AND LIMITATIONS OF CABLE BACTERIA

With their internal electric wires, cable bacteria should have privileged access to electron donorsand acceptors wherever oxic-anoxic interfaces or other redox clines are stabilized. As for any otherbacteria, intrinsic metabolic and physical limits as well as competitors, grazers, and parasites willalso create constraints on them.

Competition for Sulfide and Oxygen

In the benthic microbial environment, sulfide is a precious electron donor with a low redoxpotential, and aerobic oxidation of sulfide can be the process by which most of the energy fromorganic matter mineralization eventually becomes available (Fenchel et al. 2012). Among thegreat diversity of sulfide-oxidizing bacteria, the filamentous forms in the Beggiatoacea family areprobably the most direct competitors to cable bacteria. In marine sediments, they establish orexploit existing spatial separations of oxygen reduction and sulfide oxidation (Mussmann et al.2003, Preisler et al. 2007). Near the sediment-water interface, they incorporate nitrate in vacuolesand migrate with it to depths where sulfide is available (Sayama et al. 2005). The sulfide is partlyoxidized to elemental sulfur, which inside other vacuoles is transported back to the surface andoxidized completely to sulfate with oxygen or nitrate. Like the cable bacteria, they proliferate insediments with high rates of sulfate reduction, and observations from Tokyo Bay indicate thatthe two groups may have complementary seasonal cycles controlled by the availability of nitrate,oxygen, and sulfide (Sayama 2011).

Single-cell sulfide oxidizers proliferate when oxygen and sulfide coexist in an overlapping zone.Even in that situation, a cable bacterium may have an advantage because all cells in the filamentcan remain metabolically active as long as the filaments intersect or at least have some cells inthe overlapping zone. Should the overall limiting factor be the availability of oxygen rather thansulfide, the separation might not be established, and cable bacteria could have a persistent activitybarely detectable by present geochemical indicators.

Staying Connected

Cable bacteria’s dependence on distant resources makes it crucial for them to maintain the integrityand positions of their filaments. As directly illustrated in cutting experiments, cable bacteria aresensitive to mechanical stress (Pfeffer et al. 2012). Measurements of in situ activity and experimentshave also shown that electric currents are not detectable near bioturbating lugworms (Arenicolamarina), probably owing to filament breakage and frequent burial by sediment overturning (Malkinet al. 2014).

In general, strong selection forces should promote the length, conductivity, strength, andmotility of living electric cables (Schauer et al. 2014). Compared with the large variability in



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sampling sites, oxygen consumption rates, and current densities, the consistent sizes of the oxygen-sulfide separation zones formed by cable bacteria is striking. Across all published experiments andobservations, the zone develops to a width of approximately 10–20 mm (Table 1 and referencestherein). The low outlier of 7 mm (Schauer et al. 2014) might be related to the predominance ofthe diffusing sulfide source in that experiment, which eases the pressure to extend at depth. Thehigh outlier of 25 mm (Risgaard-Petersen et al. 2014) could be due to sulfide consumption at thesulfide boundary by iron sulfide precipitation rather than anodic oxidation, as discussed above.Time-series studies indeed suggest that the cable bacteria community begins to vanish before thegap exceeds 2 cm (Schauer et al. 2014). Are these uniform working distances a coincidence, or dothey result from intrinsic limitations in the length and conduction mode of cable bacteria?

Metabolic Scope

Even if sulfide is the sole electron donor for cable bacteria, they could still monopolize the largershare of the energy release in marine sediment processes. In coastal waters, sulfate reduction is themajor pathway of organic matter oxidation, and the standard free energy from the aerobic oxidationof the generated sulfide is five times larger than the standard free energy from the sulfate reductionitself (Thauer et al. 1977). The closest relative of identified cable bacteria is Desulfobulbus propionicus,which is well described as a sulfate reducer (Dworkin et al. 2007). Whether cable bacteria sharethis metabolism is not known, but if they do, sulfate reduction may be a secondary option whenthey lose their connection to the oxic zone. Another possibility is that sulfate reduction offers anindirect pathway for electrons from organic substrates to the anode process via sulfide.

A preliminary estimate based on time-series studies of cable bacteria biovolumes and electriccurrents indicated that cable bacteria may have high growth efficiencies, with carbon assimilationrates similar to oxygen reduction rates (Schauer et al. 2014). Whether the carbon source is organicor inorganic is not settled, and the results of a mass balance study were conflicting (Risgaard-Petersen et al. 2012): A good match between sulfide oxidation and minimum cathodic oxygenreduction (61 ± 8 and 66 ± 7 mmol electrons m−2 d−1, respectively) does not leave any significantflow of electrons for CO2 reduction, whereas a small and similar sulfate reduction rate (0.2 mmolS m−2 d−1) in the active anodic zone and in nonactive zones of similar thickness does not indicateany major drain of organic carbon for assimilation. Much more detailed studies will be needed todetermine how efficiently, when, and with what carbon sources cable bacteria can grow.

The spatial separation of oxidation and reduction process raises the intriguing and apparentlyunaddressed question of how energy is shared between anodic and cathodic cells. Another commonquestion is whether intermittent cells could somehow tap energy from the electric current, whichwould imply that they do not metabolize any external electron donors or acceptors themselves.Indeed, electric currents and cable bacteria have been established through glass bead layers, whereno electron donors or acceptors should be available (Pfeffer et al. 2012). A more trivial explanationof this would be that they make do with energy storage in combination with motility (Schaueret al. 2014).

FINDING ELECTRIC CURRENTS AND CABLE BACTERIA IN NATURE

Electric currents in marine sediments were first discovered in laboratory incubations of sulfidicsediment (Nielsen et al. 2010). Based on these results, it was proposed that electric currentsflourish in sediments where oxygen is reintroduced after oxygen depletion of the bottom waterhas excluded benthic animals and promoted sulfide accumulation. The first report on both cablebacteria and electric currents in situ appeared only recently and immediately suggested a morewidespread and persistent occurrence (Malkin et al. 2014). The geochemical signatures of electric



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currents as well as results from scanning electron microscopy and fluorescence in situ hybridizationconfirmed that cable bacteria were present at all three sampling times during a year and at threeof the four selected locations in the southern coastal North Sea area. The three locations withcable bacteria were an intertidal salt marsh, a seasonally hypoxic basin, and a subtidal coastalmud plains; the other location was sandy and heavily bioturbated by lugworms (Arenicola marina).Follow-up experiments confirmed that mechanical disruption by the worms and/or burial beneaththeir frequent surface deposits most likely eliminated the cable bacteria.

Signatures of electric currents or cable bacteria based on data from different reports in theliterature further indicate a widespread and broad diversity of marine sediments featuring electriccurrents (Malkin et al. 2014). The data encompass five locations showing the geochemical signatureof long-distance electron transport, four locations containing 16S rRNA gene sequences highlysimilar (>97%) to those of the filamentous Desulfobulbaceae, and the three sites sampled in theMalkin et al. (2014) study containing both signatures. The distinct pH signature is also evident incores collected and analyzed within three to five days in a recent study at station M5 in Aarhus Bayand in Limfjorden, Denmark (Behrendt et al. 2013). The sites vary from hypoxic ocean basins,hydrothermal vent areas, and cold seeps to eutrophic temperate and subtropical coastal areas, tidalflats, and mangroves. Their common traits are high rates of sulfide generation in muddy sedimentsand limited bioturbation (Malkin et al. 2014).

The tolerance of cable bacteria to different environmental stress factors is well illustrated bythe finding of lasting and active communities in an intertidal salt marsh (Malkin et al. 2014). Thecombination of flooding at high tide and exposure to rain or desiccation at low tide implies radicalvariation in salinity, and changes from darkness to sunshine induce both light and oxygen stress.The combination of flooding and light variability also causes significant temperature oscillations.

Various measurements have indicated that electric currents may control a significant part (andin some cases the majority) of benthic microbial metabolism. Using pH profiles and knowledge ofbuffering solute concentrations at the sediment-water interface, one can calculate rates of protonconsumption and/or alkalinity generation in the oxic zone (Malkin et al. 2014, Nielsen et al.2010). By combining these rates with the total oxygen consumption rate, one can then calculate aminimum rate of cathodic oxygen reduction, assuming that all other oxygen-reducing processesproduce at least one proton per O2 molecule reduced in the observed pH range (Nielsen et al.2010). In published experimental studies, cathodic oxygen reduction varies from 42% to at least82% of the total sediment oxygen consumption, and in freshly collected field samples it variesfrom 8% to 34% (Table 1 and references therein).

Given that estimates of the importance of electric currents are available from only 4 locations(Malkin et al. 2014) and that signatures of the presence of electric currents have been demon-strated at only another 11 marine sites (as discussed above), one can only speculate on the globalimportance of electric currents for marine biogeochemistry. No data have ruled out the possi-bility that these currents are a ubiquitous phenomenon, and it should be noted that the presenthallmark—a pH peak in the oxic zone—is present only when the electric currents make a significantcontribution to sediment metabolism and lead to net alkalinity generation by the sediment.

Regardless of the involvement of electric currents, we still have little exact knowledge about thefate of oxygen in the sea bottom. Only a few studies have succeeded in completing a benthic oxygenconsumption budget based on measures of the specific reaction and transport processes; to ourknowledge, the only examples are extreme cases, where more than 90% of the oxygen consumptionwas ascribed either to the oxidation of sulfide diffusing up from sulfate reduction in highly loadedsediments (e.g., Jørgensen & Postgate 1982) or to direct aerobic oxidation of organic matter inultraoligotrophic sediments with no anoxic zone (e.g., Røy et al. 2012). In all other cases, theoxygen bookkeeping was completed by differences or modeling, with the assumption that direct



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and indirect aerobic oxidation processes will eventually balance the mineralization of organicmatter with minor corrections for the burial of reduced sulfur and efflux of dinitrogen (Glud2008). In the microbial ecology course at our department, we had for many years a laboratoryexercise aiming at a complete mass balance for the cycling of carbon, sulfur, nitrogen, iron, andoxygen in three-week incubations of homogenized sediment collected from station M5 in AarhusBay. The oxygen budget never fit, and the poor students (and teachers) were blamed for badperformance or choice of methods. After reinspection of the data and repetitions with pH profilesincluded, it appears that electric currents were the only missing link.

SUMMARY POINTS

1. Electric currents in marine sediments may link oxidation and reduction processes overdistances beyond 2 cm.

2. Electric currents may drive a significant share of the benthic oxygen consumption insediments where sulfate reduction dominates carbon mineralization.

3. The electric currents are driven by cable bacteria characterized as multicellular, filamen-tous bacteria with electron-transporting structures inside a common periplasm.

4. The documented electron sources in marine sediments are pore-water sulfide diffusing upfrom sulfate reduction in underlying zones, sulfide produced locally by sulfate reduction,and sulfide produced by iron sulfide dissolution. The documented electron sinks areoxygen and nitrite.

5. The presence of these electric currents requires rethinking several aspects of biogeo-chemistry: (a) Reacting electron donors and acceptors can be centimeters apart. (b) Theseparation of oxidation and reduction processes generates pH extremes. Protons fromanodic sulfide oxidation drive extensive carbonate dissolution, with potential implica-tions for ocean acidification and CO2 uptake. (c) Anodic depletion of sulfide may elicitsubstantial mobilization and migration of ferrous iron from iron sulfide. (d ) Microbialelectric fields influence the migration and distribution of all ions in sediment.

6. The surprise discovery of electric currents and cable bacteria at well-studied marinelocations reminds us of how much remains to be found and the importance of keepingan open mind.

FUTURE ISSUES

1. The emergence and role of microbial electric currents in Earth’s history and their im-prints in the geological record remain unknown.

2. The mobilization, migration, and stabilization of minerals by microbial electric currentshave not been determined.

3. Investigators should search for other types of cable bacteria, including phototrophs andorganotrophs.

4. Better tools are needed for detecting and measuring microbial electric currents and theireffects.



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5. The ranges of habitats, seasons, distances, electron donors, and electron acceptors ofmicrobial electric currents have not been determined.

6. The associations and syntrophy between cable bacteria and other organisms should beelucidated.

7. Electrons should be incorporated into biogeochemical models.

DISCLOSURE STATEMENT

The authors are not aware of any affiliations, memberships, funding, or financial holdings thatmight be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS

We thank colleagues in the Section of Microbiology, Department of Bioscience, Aarhus Uni-versity, and in Club Electro for discussions of and input into this review. Our research receivedfunding from the European Research Council under European Union Seventh Framework Pro-gram grant FP/2007-2013/European Research Council Grant Agreement 291650 (to L.P.N.) aswell as from Danish National Research Foundation grant DNRF104 (to N.R.-P.).

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rethinking sediment biogeochemistry after the discovery of electric currents

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